REVIEWS Master recyclers: features and functions of bacteria associated with phytoplankton blooms Alison Buchan1, Gary R. LeCleir1, Christopher A. Gulvik2 and José M. González3 Abstract | Marine phytoplankton blooms are annual spring events that sustain active and diverse bloom-associated bacterial populations. Blooms vary considerably in terms of eukaryotic species composition and environmental conditions, but a limited number of heterotrophic bacterial lineages — primarily members of the Flavobacteriia, Alphaproteo- bacteria and Gammaproteobacteria — dominate these communities. In this Review, we discuss the central role that these bacteria have in transforming phytoplankton-derived organic matter and thus in biogeochemical nutrient cycling. On the basis of selected field and laboratory-based studies of flavobacteria and roseobacters, distinct metabolic strategies are emerging for these archetypal phytoplankton-associated taxa, which provide insights into the underlying mechanisms that dictate their behaviours during blooms. Autotrophs Phytoplankton, such as diatoms and coccolithophores, in a patchy distribution of bacterial activity throughout 6 Organisms that convert are free-floating photosynthetic organisms that are the oceans . Copiotrophic bacteria, which swiftly capital- inorganic carbon, such as CO2, found in aquatic environments. These organisms capture ize on increased carbon and nutrient concentrations at into organic compounds. energy from sunlight and transform inorganic matter both the microscale and macroscale, complement their Biological pump into organic matter (which is known as biomass). In the oligotrophic counterparts, which prefer dilute nutrient The export of phytosynthetically ocean, this organic matter is the foundation of a com- concentrations. Together, the heterotrophic bacteria, derived carbon via the sinking plex marine food web, which relies heavily on microbial which use these two distinct trophic strategies balance of particles from the illuminated transformation: approximately one-half of the carbon marine productivity. surface ocean to the deep that is fixed by marine autotrophs is directly processed by Microbially transformed carbon has several possible ocean. Approximately 0.1% of 1,2 (FIG. 1) the carbon that is fixed in the bacteria . The remaining carbon either enters the classic fates in the ocean ; for example, microbial respira- ocean is buried in marine marine food web or is transported as sinking particles tion converts carbon to an inorganic, gaseous state as sediments via this process. biological to the deep ocean for long-term storage via the CO2 that is released into the atmosphere. Phytoplankton- pump3 (FIG. 1). Localized and transient increases in the derived carbon can also enter the microbial loop, where it abundance of phytoplankton are referred to as blooms is first converted into microbial biomass and can either 1Department of Microbiology, and result in a boost in biogeochemical activities, includ- be transferred up the food web as bacteria succumb to University of Tennessee, ing the assimilation of CO2 and inorganic nutrients, predation by organisms at higher trophic levels (such Knoxville, Tennessee 4,5 37996-0845, USA. such as nitrogen and phosphorus . These processes are as zooplankton) or remain in the microbial domain 7 2School of Civil and partly balanced by a subsequent increase in the activity of via continual recycling . Alternatively, a fraction of the Environmental Engineering, heterotrophi­c bacteria, which transform phytoplankton- microbially transformed carbon is released into the dis- Georgia Institute of derived organic matter. As phytoplankton blooms are solved phase, some of which resists degradation and Technology, Atlanta, Georgia 30332, USA. often seasonal in nature and are thus transient events, contributes to the large pool of recalcitrant dissolved 3Department of Microbiology, the abundance and activity of heterotrophic bacteria organic carbon (DOC) that is stored in the ocean for University of La Laguna, varies accordingly. Indeed, secondary bacterial pro- thousands of years via the microbial carbon pump8. In ES-38200 La Laguna, Spain. duction typically correlates with the concentration addition, bacteria also regenerate nutrients that are Correspondence to A.B. of chlorophyll a, which is a proxy for phytoplankton associated with phytoplankton organic matter, particu- e-mail: [email protected] 2 7 doi:10.1038/nrmicro3326 abundance . This correlation between primary and larly nitrogen and phosphorus . Although it is not dis- Published online secondary production is evident on both small (that is, cussed in depth here, viral lysis of heterotrophic bacteria 19 August 2014 micromolar) and large (that is, basin) scales and results and phytoplankton is an important mechanism for the 686 | OCTOBER 2014 | VOLUME 12 www.nature.com/reviews/micro © 2014 Macmillan Publishers Limited. All rights reserved REVIEWS CO2 Bacteria–phytoplankton interactions during bloom events are complex and change throughout the lifetime CO of the bloom. Bacteria can support the growth of phyto- 2 CO 2 plankton via the recycling of nutrients, but at the same time, they also compete with phytoplankton for essen- tial nutrients. Both healthy and dead (or dying) phyto- 1 Phytoplankton Zooplankton plankton release organic compounds that are consumed 3 by heterotrophic bacteria, and the chemical nature and concentration of the released compounds varies with phytoplankton species and the physiological status of the phytoplankton10,11. Phytoplankton species show vari- 2 ation in their biochemical composition and the relative DOM POM cellular proportions of proteins, fatty acids, sugars and nucleic acids12–14. This variation in composition influ- DOC, DON and DOP POC, PON and POP ences both the stoichiometry, such as the C/N/P ratio, 4 and bioreactivity of phytoplankton-derived POM and Microbial loop DOM, which in turn influences the metabolic activity and proliferation of heterotrophic bacteria and dictates Heterotrophic their growth efficiencies as well as the fate of microbially P bacteria 6 P transformed organic matter . N P N Despite the variation in phytoplankton composition N and environmental conditions, a limited number of taxa Inorganic nutrients are consistently found to dominate bloom-associated Biological bacterial communities. The most frequent bacteria that pump 6 Microbial are identified by 16S ribosomal RNA gene-based sur- carbon pump 5 veys are members of the classes Flavobacteriia (hereafter 7 Viral shunt referred to as flavobacteria), Alphaproteobacteria, includ- ing members of the Rhodobacteraceae (such as roseo- bacters), and Gammaproteobacteria, such as members Long-term storage of the Alteromonadaceae15–17. The metabolic properties Figure 1 | Bacterial transformation of phytoplankton-derivedNature Reviews organic | Microbiology matter. The of these bacteria enable their ready response to transient marine carbon cycle includes a number of processes, several of which are mediated by nutrient pulses, which are a hallmark of phytoplankton microorganisms. Key processes of the marine carbon cycle include the conversion of blooms. Moreover, several laboratory studies have iden- inorganic carbon (such as CO2) to organic carbon by photosynthetic phytoplankton tified specific associations between phytoplankton and species (step 1); the release of both dissolved organic matter (DOM; which includes certain species of roseobacters and flavobacteria. As such, dissolved organic carbon (DOC), dissolved organic nitrogen (DON) and dissolved organic these two bacterial groups have emerged as the main phosphorous (DOP)) and particulate organic matter (POM; which includes particulate models for the study of microorganism–phytoplankton organic carbon (POC), particulate organic nitrogen (PON) and particulate organic phosphorous (POP)) from phytoplankton (step 2); the consumption of phytoplankton interactions. This Review provides a brief overview of marine biomass by zooplankton grazers (step 3) and the mineralization (that is the release of CO2 via respiration during the catabolism of organic matter) and recycling of organic matter phytoplankton blooms and highlights recent advances by diverse heterotrophic bacteria, including, but not limited to, flavobacteria and in our understanding of the composition, dynamics and roseobacters (which is known as the microbial loop; step 4). A fraction of the physiologies of bloom-associated bacteria. Owing to the heterotrophic bacteria is consumed by zooplankton, and the carbon is further variation in the types of naturally occurring blooms, it transferred up the food web. Heterotrophic bacteria also contribute to the is difficult to depict a generalized bloom scenario that remineralization of organic nutrients, including DON and DOP, to inorganic forms, adequately encompasses the complexity of all of the which are then available for use by phytoplankton. The microbial carbon pump (step 5) observed systems. Instead, the objective here is to pro- refers to the transformation of organic carbon into recalcitrant DOC that resists further vide an overview of the most common bloom events and degradation and is sequestered in the ocean for thousands of years. The biological pump (step 6) refers to the export of phytoplankton-derived POM from the surface oceans to describe our understanding of microbial–phytoplankto­n deeper depths via sinking. Finally, the viral shunt (step 7) describes the contributions of interactions for flavobacteria and roseobacters,